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Architectural Design Drives the Biogeography of Indoor

Bacterial Communities
Steven W. Kembel
1,2,3.
, James F. Meadow
2,3
*
.
, Timothy K. OConnor
2,3,4
, Gwynne Mhuireach
2,5
,
Dale Northcutt
2,5
, Jeff Kline
2,5
, Maxwell Moriyama
2,5
, G. Z. Brown
2,5,6
, Brendan J. M. Bohannan
2,3
,
Jessica L. Green
2,3,7
1De partement des sciences biologiques, Universite du Que bec a` Montreal, Montre al, Quebec, Canada, 2Biology and the Built Environment Center, University of Oregon,
Eugene, Oregon, United States of America, 3Institute of Ecology and Evolution, University of Oregon, Eugene, Oregon, United States of America, 4Department of Ecology
and Evolutionary Biology, University of Arizona, Tucson, Arizona, United States of America, 5Energy Studies in Buildings Laboratory, University of Oregon, Eugene,
Oregon, United States of America, 6Department of Architecture, University of Oregon, Eugene, Oregon, United States of America, 7Santa Fe Institute, Santa Fe, New
Mexico, United States of America
Abstract
Background: Architectural design has the potential to influence the microbiology of the built environment, with
implications for human health and well-being, but the impact of design on the microbial biogeography of buildings remains
poorly understood. In this study we combined microbiological data with information on the function, form, and
organization of spaces from a classroom and office building to understand how design choices influence the biogeography
of the built environment microbiome.
Results: Sequencing of the bacterial 16S gene from dust samples revealed that indoor bacterial communities were
extremely diverse, containing more than 32,750 OTUs (operational taxonomic units, 97% sequence similarity cutoff), but
most communities were dominated by Proteobacteria, Firmicutes, and Deinococci. Architectural design characteristics
related to space type, building arrangement, human use and movement, and ventilation source had a large influence on the
structure of bacterial communities. Restrooms contained bacterial communities that were highly distinct from all other
rooms, and spaces with high human occupant diversity and a high degree of connectedness to other spaces via ventilation
or human movement contained a distinct set of bacterial taxa when compared to spaces with low occupant diversity and
low connectedness. Within offices, the source of ventilation air had the greatest effect on bacterial community structure.
Conclusions: Our study indicates that humans have a guiding impact on the microbial biodiversity in buildings, both
indirectly through the effects of architectural design on microbial community structure, and more directly through the
effects of human occupancy and use patterns on the microbes found in different spaces and space types. The impact of
design decisions in structuring the indoor microbiome offers the possibility to use ecological knowledge to shape our
buildings in a way that will select for an indoor microbiome that promotes our health and well-being.
Citation: Kembel SW, Meadow JF, OConnor TK, Mhuireach G, Northcutt D, et al. (2014) Architectural Design Drives the Biogeography of Indoor Bacterial
Communities. PLoS ONE 9(1): e87093. doi:10.1371/journal.pone.0087093
Editor: Bryan A. White, University of Illinois, United States of America
Received July 18, 2013; Accepted December 18, 2013; Published January 29, 2014
Copyright: 2014 Kembel et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This research was funded by a grant to the Biology and the Built Environment Center from the Alfred P. Sloan Foundation Microbiology for the Built
Environment Program (http://www.sloan.org/major-program-areas/basic-research/microbiology-of-the-built-environment/). The funders had no role in study
design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: jfmeadow@gmail.com
. These authors contributed equally to this work.
Introduction
Biologists and designers are beginning to collaborate in a new
field focused on the microbiology of the built environment [1,2].
These collaborations, which integrate perspectives from ecology
and evolution, architecture, engineering and building science, are
driven by a number of interrelated observations. First, it is
increasingly recognized that buildings are complex ecosystems
comprised of microorganisms interacting with each other and their
environment [35]. Second, the built environment is the primary
habitat of humans; humans spend the majority of their lives
indoors where they are constantly coming into contact with the
built environment microbiome (the microbial communities within
buildings) [6]. Third, evidence is growing that the microbes living
in and on people, the human microbiome, play a critical role in
human health and well-being [79]. Together, these observations
suggest that it may be possible to influence the human microbiome
and ultimately human health, by modifying the built environment
microbiome through architectural design.
Despite this potential, we remain in the very early stages of
understanding the link between design and the microbiology of the
indoor environment. A comprehensive understanding of the
mechanisms that shape indoor ecosystems will entail disentangling
the relative contributions of biological processes including
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environmental selection, dispersal, diversification, and ecological
drift [10]. To date, most research has focused on understanding
the influence of environmental selection and dispersal on the built
environment microbiome. Environmental conditions including
humidity and air temperature have been shown to influence the
growth rate and survival of many microbial taxa [3,5,11] and
correlate with the composition of bacterial communities indoors
[4]. Many bacteria and fungi exhibit strong microhabitat
associations and increased growth under conditions of higher
humidity and in the presence of water sources, such as in kitchens
and restrooms [12,13]. The dispersal of microbes into and within
the built environment also appears to have a significant influence
on indoor ecosystems. The sources of microbes include those from
outdoor habitats such as air and soil brought into the building via
ventilation systems or carried into the building by macroorganisms
[4,1416], microbes from indoor sources such as water, carpets
and other surfaces within a building [13,17], and microbes emitted
from macroorganisms within the building including humans, pets
and plants [18,19]. The relative importance of these different
sources of microbes indoors is not well understood, but is likely to
differ as a function of space (e.g. geographic location [20]), time
(e.g. year and season of sampling [15]), and building design and
operation [4].
The biological processes described above can be fundamentally
altered by building design. However many questions remain
unanswered regarding how design aspects such as the function,
form and organization of a building - shape the indoor microbiome.
Function refers to the collection of activities and uses that a building
and its spaces serve. Functional requirements are translated into
the variety and number of space types within a building for
example offices, restrooms, and hallways. Function is also a key
determinant of the design criteria for environmental conditions
including temperature, relative humidity, and light levels. Form
refers to geometry of a building and the spaces within it, while
organization refers to the spatial relationships among indoor spaces.
Form and organization are highly interrelated and both involve
design choices that influence human circulation (the source,
variation and movement of people), air circulation (the source,
variation and movement of air), and environmental conditions
throughout a building.
To understand how design choices influence the biogeography
of indoor bacterial communities, we collected microbiological,
architectural, and environmental data in 155 rooms throughout a
multi-use classroom and office building (Lillis Hall; Fig. 1). We
focus on the bacterial communities in settled dust, because it
represents an integrative record of microbial biodiversity in indoor
Figure 1. Architectural layout for two of four floors in Lillis Hall. Restrooms (brown), offices (blue) and classrooms (yellow) are shown to
illustrate space type distribution throughout Lillis. The first two floors of the building are primarily devoted to classrooms and share a similar floor-
plan. The 3rd and 4th floors contain most offices in the building and also share a similar floor-plan. The building has a basement and penthouse
spaces; these are largely building support spaces, including mechanical rooms and storage.
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spaces [21]. Our study addresses two overarching questions. First,
at the scale of the entire building, do function, form and
organization predict variation in the built environment micro-
biome? Second, for rooms that serve the same function (rooms that
are of the same space type), which aspects of form and
organization most influence the built environment microbiome?
Methods
Study Location
We analyzed bacterial communities in dust collected from 155
spaces in the Lillis Hall, a four-story classroom and office building
on the University of Oregon campus in Eugene, Oregon, USA.
This building was chosen as a study site for several reasons.
Architecturally, Lillis Hall was designed to accommodate natural
ventilation for both fresh air and cooling; the building is thin,
allowing most rooms access to the building skin for supplying
outside air directly through windows and louvers, and it has a
central atrium used for exhausting air through stack ventilation.
From a study design perspective, diverse space types, occupancy
levels, and building management strategies were located in close
proximity within the same building, making it possible to compare
their relative influences on indoor biogeography.
Architectural Design Data
Data on architectural design attributes of each space including
function, form, and organization were obtained using architectural
plans, field observation, and a building information model (Fig. 1).
Spaces in the building were classified into one of seven space types.
This classification system was developed for the present study
based on the Oregon University Systems space type codes and
definitions [40]. These categories are based on the overall
architectural design and intended human use pattern for each
space, and include circulation (e.g. hallways, atria), classrooms,
classroom support (e.g. reading and practice rooms), offices, office
support (e.g. most storage spaces, conference rooms), building support
(e.g. mechanical equipment rooms, janitor closets), and restrooms.
We measured numerous spatial and architectural attributes of
each space including level (floor), wing (east versus west), size (net
floor area), air handling unit (AHU) (13 different AHUs supply air to
different rooms, so AHU is a categorical variable with 15 levels,
one for each AHU as well as a none category for rooms without
mechanically supplied air, and a multiple category for circulation
spaces fed by multiple supply sources), and a separate binary
variable denoting whether the space was only capable of being
naturally ventilated by unfiltered outside air (e.g. via windows or
louvers; 41 rooms) or by dedicated mechanical AHU supply (114
rooms).
Figure 2. Network analysis metrics used to quantify spatial arrangement of spaces within Lillis Hall. Examples in the left column follow
classic network representation, while those in the right column embody the architectural translation of networks. Shaded nodes and building spaces
correspond to centrality measures [22] of betweenness (the number of shortest paths between all pairs of spaces that pass through a given space over
the sum of all shortest paths between all pairs of spaces in the building) and degree (the number of connections a space has to other spaces);
connectance distance (the number of doors between any two spaces) is a pairwise metric, shown here as the range of connectance distance values for
each complete network/building. Since betweenness and degree strongly co-vary and are both measures of network centrality [22], they are
considered together in some analyses.
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Metrics related to form and organization were quantified using
network analysis (Fig. 2) and information from building construc-
tion drawings. Spaces were considered to be spatially connected if
they shared a doorway or other physical connection that would
permit a person to move directly between the two spaces. The
network of spatial connections among spaces was used to calculate
two measures of network centrality [22,41] for each space in the
building: betweenness, a measure of the fraction of shortest paths
among all spaces in the building that would pass through a space,
and degree, the number of connections a space has to other spaces.
The network of spatial connections between spaces was also used
to define a connectance distance between all pairs of spaces in the
building, defined as the minimum number of spaces a person
would need to travel through to move between two spaces. We
considered using ventilation-based distance (how much duct length
separates two connected spaces) as a connectance distance,
however preliminary investigation indicated that connectance
distance and ventilation distance were strongly correlated.
Human use patterns are a product of functional classification,
but they also dictate form and organizational attributes of building
design. In this study, human use patterns for each space were
estimated based on a qualitative assessment of the expected
patterns of human diversity and annual occupied hours in each space.
Briefly, human diversity was defined on a three-point scale,
ranging from low human diversity (spaces likely to be occupied by
at most a single individual during a typical day; e.g. a closet) to
high human diversity (spaces likely to be occupied by numerous
different individuals during a typical day; e.g. a hallway). Annual
occupied hours (person-hours per year) were similarly defined
along a three-point scale from low (spaces that are typically vacant
or occupied at low density; e.g. a mechanical support space) to
high (spaces that are frequently occupied at relatively high density;
e.g. administrative offices). Both of these human occupancy
variables are explained in more detail in Table S1.
At the time of microbial community sampling, ambient air
temperature and relative humidity measurements were taken from
each space. Relative humidity measurements were detrended
using daily mean values to account for temporal changes over the
sampling period.
Figure 3. The taxonomic composition of bacterial communities sampled from dust in Lillis Hall. Samples are organized by space type,
and relative abundances are shown for groups comprising more than 1% (for phylum and class level) and 4% (for order level).
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Biological Sampling
Sampling of dust was carried out with a Shop-VacH 9.4L Hang
Up vacuum (www.shopvac.com; #215726) fitted with a Dus-
tream
TM
Collector vacuum filter sampling device (www.inbio.
com/dustream.html). Dust samples were collected by vacuuming
an area of approximately 2m
2
on horizontal surfaces above head
level for 2 minutes in each space. We preferentially chose these
surfaces for sampling since they minimized the frequency of
disturbance by cleaning, and thus likely serve as a long-term
sample of airborne particles in each space [21]. All samples were
collected during June 2224, 2012. Building construction was
completed in 2003, and dust has presumably been accumulating in
some sampled spaces since that time.
Dust samples were stored at 280uC until DNA extraction. Dust
was manually extracted from filters, and used for DNA extraction.
Whole genomic DNA was isolated from samples using MO BIO
PowerLyzer
TM
PowerSoilH DNA Isolation Kit (MO BIO,
Carlsbad, CA) according to manufacturers instructions with the
following modifications: bead tubes were vortexed for 10 min;
solutions C4 and C5 were substituted for PW3 and PW4/PW5
solutions from the same manufacturers PowerWaterH DNA
isolation kit. Bacterial communities were profiled by sequencing
a ,420 bp fragment of the V4 region of the bacterial 16S rRNA
gene using a custom library preparation protocol [24]. Briefly, the
protocol consisted of two PCRs. The first amplified the V4/V5
region using the primers 59-AYTGGGYDTAAAGNG-39 and 59-
CCGTCAATTYYTTTRAGTTT-39 [42,43] and appended a
6 bp barcode and partial Illumina sequencing adaptor. Forward
and reverse strands were labeled with different barcodes, and the
unique combination of these barcodes was used to pool samples in
post-processing.
All extracted samples were amplified in triplicate for PCR1 and
triplicates were pooled before PCR2. PCR1 (25 mL total volume
per reaction) consisted of the following ingredients: 5 mL 5x HF
buffer (Thermo Fisher Scientific, U.S.A.), 0.5 mL dNTPs (10 mM),
0.25 mL Phusion Hotstart II polymerase (Thermo Fisher Scien-
tific, U.S.A.), 13.25 mL certified nucleic-acid free water, 0.5 mL
forward primer (10 uM), 0.5 mL reverse primer (10 uM), and 5 mL
template DNA. The PCR1 conditions were as follows: initial
denaturation for 30 s at 98uC; 20 cycles of 20 s at 98uC, 30 s at
50uC and 30 s at 72uC; and 72uC for 10 min for final extension.
After PCR1, the triplicate reactions were pooled and cleaned with
the QIAGEN Minelute PCR Purification Kit according to the
manufacturers protocol (QIAGEN, Germantown, MD). Amplified
products from PCR1 were eluted in 11.5 mL of Buffer EB. For
PCR2, a single primer pair was used to add the remaining
Illumina adaptor segments to the ends of the concentrated
amplicons of PCR1. The PCR2 (25 mL volume per reaction)
consisted of the same combination of reagents that was used in
PCR1, along with 5 mL concentrated PCR1 product as template.
The PCR 2 conditions were as follows: 30 s denaturation at 98uC;
15 cycles of 10 s at 98uC, 30 s at 64uC and 30 s at 72uC; and
10 min at 72uC for final extension.
Amplicons were size-selected by gel electrophoresis: gel bands at
c. 500bp were extracted and concentrated, using the ZR-96
Zymoclean Gel DNA Recovery Kit (ZYMO Research, Irvine,
CA), following manufacturers instructions, quantified using a
Qubit Fluorometer (Invitrogen, NY), and pooled in equimolar
concentrations for library preparation for sequencing. Resulting
libraries were sequenced in two multiplexed Illumina MiSeq lanes
(paired-end 150 base pair sequencing) at the Dana Farber Cancer
Institute (Boston, MA). All sequence data and metadata have been
deposited in the open-access data repository Figshare (http://
figshare.com/articles/Lillis_Dust_Sequencing_Data/709596).
Sequence Processing
We processed raw sequence data with the FastX_Toolkit (http://
hannonlab.cshl.edu/fastx_toolkit) and QIIME [44] software pipe-
lines to eliminate low-quality sequences and de-multiplex sequenc-
es into samples. Sequences were trimmed to a length of 200 bp
(100 bp from each paired end). We retained sequences with an
average quality score of 30 over 97% of the sequence length after
trimming. After trimming, quality filtering and rarefaction of each
sample to 2,100 sequences to ensure equal sampling depth across
samples, 329,700 sequences from 155 samples remained and were
included in all subsequent analyses. We binned sequences into
operational taxonomic units (OTUs) at a 97% sequence similarity
cutoff using UCLUST [45] and assigned taxonomy to each OTU
using the BLAST taxon assignment algorithm and Greengenes
version 4feb2011 core set [46] as implemented in QIIME version
1.4. We inferred phylogenetic relationships among all bacterial
OTUs using a maximum likelihood GTR+Gamma phylogenetic
model in FastTree [47].
Data Analysis
Statistical analysis was performed in R [48]. Pairwise commu-
nity dissimilarity was calculated using the quantitative, taxonomy-
based Canberra distance metric, implemented in the vegan package
Table 1. Variance in biological dissimilarity among bacterial
communities from all spaces, as well as just offices, (Canberra
distance) explained by different variables in Lillis Hall.
Room types Explanatory variable R
2
P-value
all rooms Space type 0.06 0.001
Air source - air handling unit (AHU) 0.13 0.001
Building floor 0.01 0.001
Space size 0.01 0.001
Building wing - East/West 0.01 0.341
Building side - North/South 0.01 0.001
Occupant diversity 0.01 0.001
Annual occupied hours 0.01 0.015
Centrality (betweenness) 0.01 0.001
Centrality (degree) 0.01 0.001
Temperature 0.01 0.024
Relative Humidity* 0.01 0.001
Natural ventilation capability 0.01 0.001
offices Air source - air handling unit (AHU) 0.07 0.001
Building floor 0.07 0.001
Space size 0.02 0.025
Building wing - East/West 0.01 0.541
Centrality (betweenness) 0.02 0.005
Centrality (degree) 0.02 0.016
Temperature 0.02 0.002
Relative Humidity* 0.01 0.786
Natural ventilation capability 0.02 0.001
Variance explained (R
2
) and statistical significance (P-value) quantified with a
PERMANOVA test; since P-values are from permutational tests involving 999
permutations, they are only reported down to 0.001. All variables and their
respective units are described in the methods section and Table S1.
*detrended using daily averages.
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[49] in R. We also assessed the consequences of beta-diversity
metric choice on our results; correlations between potential
metrics are included as Fig. S1. Constrained ordinations
(distance-based redundancy analysis; DB-RDA) were created
utilizing the capscale function in vegan. Correlations reported on
ordination axes, indicated by arrows, are based on simple linear
models of environmental variables against ordination axes.
Indicator taxa analysis [50] was performed using the indval
function in the labdsv package [51]. Mantel and partial mantel tests
were used to investigate the correlations between community and
environmental distance matrices, including a distance-decay
comparison, using the mantel function in vegan. Permutational
multivariate analysis of variance (PERMANOVA) was used to test
community differences between groups of samples as a way to
identify drivers of variation in community structure, using the
adonis function in vegan. All permutational tests were conducted
with 999 permutations, and thus p-values are reported down to, but
not below, 0.001.
Results
Building-scale Design Influences on the Built
Environment Microbiome
Bacterial communities in dust from Lillis Hall were highly
diverse. Using barcoded Illumina sequencing of 16S rRNA genes,
we detected 32,964 operational taxonomic units (OTUs; defined
at a 97% sequence similarity cut-off) in 791,192 sequences from
155 samples (19,403 OTUs and 325,500 sequences after
rarefaction to 2,100 sequences per sample). Most of these OTUs
were rare, occurring in one (49.9%) or two (13.3%) samples, and
at low relative abundance (61.1% of OTUs were singletons or
doubletons). However, OTUs from several taxonomic groups
including Alpha-, Beta-, and Gamma-Proteobacteria, Firmicutes,
and Deinococci were abundant and common in almost all dust
samples we collected (Fig. 3 and Fig. S2). There were 58 OTUs
belonging to these taxonomic groups that were present in 95% or
more of all samples we collected. These ubiquitous OTUs were
also abundant, representing 0.1% of the OTU richness but .28%
of all sequences.
Spaces differing in their architectural design characteristics
contained distinctive bacterial communities. Analysis of the
variance in bacterial community composition explained by
Figure 4. Dust communities within a building cluster by space type and are strongly correlated with building centrality and human
occupancy. Points represent centroids (6SE) from distance based redundancy analysis (DB-RDA). Space types hold significantly different
communities (P =0.005), though this is driven primarily by restrooms. Bacterial OTUs that have the strongest influence in sample dissimilarities are
shown at the margins; numbers in parentheses indicate multiple OTUs in the same genus. Centrality (along y-axis) represents network betweenness
and degree; human occupancy (along x-axis) represents annual occupied hours and human diversity. All four correlates (simple linear models as a
factor of ordination axis) are significant along their respective axes (all P,0.001).
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different factors (Table 1; PERMANOVA on Canberra distances)
indicated that space type and air handling unit (AHU) explained
the greatest proportion of variance (R
2
=0.06 & 0.13, respectively;
both P =0.001). Nearly all other variables considered in this study
(Table 1) were significantly correlated with biological variation as
well, but explained a far smaller portion of the overall variance in
microbial community structure at the scale of the building. Thus
Table 1 can be seen as a potential list of building features that can,
in the future, be targeted when attempting to account for
microbiological variation in architectural design.
Restrooms explained a substantial amount of the variation
observed between space types; bacterial communities in restrooms
were compositionally distinct from other space types (R
2
=0.06;
P =0.001; from PERMANOVA on Canberra distances). In
addition to serving a distinct function, restrooms were character-
ized architecturally by relatively low network centrality (quantified
as network betweenness and degree [22]; network terminology
outlined in Fig. 2). This is because in Lillis hall, restrooms
generally only have a single door and are rarely or never on a path
between any two other spaces. Restrooms also had a high diversity
of human occupants (defined as a high number of different
occupants throughout the day; explicit definitions of occupancy
variables provided in Table S1). Indicator taxa analysis detected
numerous OTUs that were associated with restrooms, predomi-
nantly belonging to taxa that are commonly associated with the
human gut and skin microbiome including Lactobacillus, Staphylo-
coccus, and Streptococcus. Taxa including Lactobacillus, Staphylococcus
and Clostridiales were also more abundant in restrooms compared
with other space types, while Sphingomonas were relatively less
abundant in restrooms (Fig. 4).
Aside from restrooms, bacterial communities in Lillis hall
tended to vary with both human occupancy and room centrality
(Fig. 4). For instance hallways, which had high human occupancy
and high occupant diversity (e.g., relatively many occupants and
many different occupants throughout the day) as well as high
centrality (hallways often serve as a pathway between rooms), were
distinct from spaces such as mechanical support rooms and faculty
offices with the opposite set of attributes (Fig. 4). While there were
few statistically significant indicator taxa from individual space
types other than restrooms, there was variation in the abundance
Figure 5. Offices contain significantly different dust microbial communities depending on ventilation source. a) The first axis is
constrained by whether or not offices have operable window louvers (blue) or not (red). Taxon names on either side are grouped from the 25
strongest weighting OTUs in either direction. b) Deinococcus were 1.7 times more abundant in mechanically ventilated offices compared to window
ventilated offices. c) The opposite pattern was observed for Methylobacterium OTUs, which were 1.8 times more abundant in window ventilated
offices. Boxplots delineate (from bottom) minimum, Q1, median, Q3, and maximum values; notches indicate 95% confidence intervals. d) Cross-
sectional view of representative Lillis Hall offices. Offices on the south side of the building (left) received primarily mechanically ventilated air, while
offices on the north side of the building (right) are equipped with operable windows as a primary ventilation air source.
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of major bacterial taxa among these spaces. Taxa including
Lactococcus, Pseudomonas, and Streptococcus were more abundant in
the centrally located and highly-occupied spaces (Fig. 4), while
Achromobacter and Methylobacterium were more abundant in the less
central and less occupied spaces. Space types did not vary
significantly in terms of their overall bacterial OTU richness or
diversity (ANOVA using rarefied OTU richness and Shannon
diversity; P =0.2 & 0.9, respectively).
Design Influences on the Built Environment Microbiome
within a Space Type
The large number of office spaces (73 offices) made it possible to
test for drivers of microbial community variation among offices.
Using a single space type also allowed us to hold relatively constant
several building parameters. Specifically, parameters including
space size, relative humidity, and occupancy varied less across
offices than across all rooms at the building-scale. Variation in
bacterial community structure among faculty offices was largely
explained by the ventilation source in offices, with mechanically
ventilated faculty offices containing a distinctive set of bacterial
taxa when compared with window ventilated faculty offices (Fig. 5;
R
2
=0.025; P =0.005). Taxa including Deinococcus, Achromonobacter,
and Roseomonas were associated with mechanically ventilated
faculty offices, while Methylobacterium, Sphingomonas, and Streptococcus
were more closely associated with window ventilated faculty
offices. Two of the most abundant of these strongly weighting taxa,
Deinococcus and Methylobacterium, when grouped by genus, show
consistent abundance differences between offices with different
ventilation strategies. We found a strong association between the
spatial connectance distance of offices (the number of doors
through which one must walk between any two spaces) versus the
microbial community similarity of offices (Fig. 6; R=0.19;
P =0.002; from a Mantel test of Canberra distance vs. spatial
connectance distance). This association was also significant at the
building scale, regardless of space type (R=0.11; P =0.001).
Discussion
In this paper we first asked: at the scale of the entire building, do
function, form and organization predict variation in the built
environment microbiome? Our data suggest that the answer is
yes. In architecture, function translates to space type, which in
Lillis Hall was the strongest predictor of microbiome variation
throughout the building. Due to the integrative nature of
architectural design, function often drives patterns in the form
and organization of spaces throughout a building, and form and
organization are necessarily difficult to disentangle. Although form
and organization are distinct aspects of architectural design, we
did not attempt to draw a distinction between them in our
analyses, since nearly every building variable herein relates to
both. In Lillis Hall, design choices resulted in distinct space types
that greatly differed in terms of their architectural characteristics,
which were related to variation in microbial community compo-
sition at the building-scale. We also focused our analyses on the
most common space type in Lillis Hall: offices. Specifically, we
asked which aspects of form and organization most influenced the
built environment microbiome in offices. We found that network
betweenness, building floor, space size, and ventilation source were
the strongest predictors for microbiome variation, even after
holding function constant.
Despite the microbiome variation across space types, we
detected a core built environment microbiome [23] of bacterial
taxa that were present in nearly every indoor space we sampled.
This core microbiome was dominated by taxa including members
of the Proteobacteria and Firmicutes that are commonly found in
indoor dust [15], although other common indoor dust taxa such as
Actinobacteria were rare in this building (c. 1% of sequences).
Many of the common taxa in the indoor dust microbiome were
also detected in air and surface samples from the same building
[24], suggesting that resuspension and settling of microbes from
these pools of potential colonists are contributing to the
communities detected in dust. The synchrony among these three
microbial pools (air, surfaces and dust) within Lillis Hall suggests a
conserved core building microbiome. Likely sources of this core
microbiome include humans, soils and plants. We found that
several of the bacterial taxa most strongly associated with
restrooms as well as with high occupant diversity space types,
such as classrooms, are also known to be associated with the
human microbiome (e.g. Lactobacillus and Staphylococcus), while
bacteria in low occupant diversity space types such as faculty
offices and mechanical support spaces were more indicative of
outdoor environments such as soils and the phyllosphere (e.g.
Methylobacterium).
There has been a recent debate regarding the relative
importance of dispersal from outdoor sources versus the conditions
within buildings for determining the structure of indoor microbial
communities [16,24,25]. We found evidence for the importance of
both types of processes: the potential for dispersal from outdoor
sources (e.g. ventilation air source, natural ventilation capacity)
and conditions within the building (e.g. space type, building floor,
temperature and relative humidity) influenced microbial commu-
nity structure. This suggests that dispersal- and niche-based
explanations will be required to understand the dynamics of the
built environment microbiome. As in any ecological community,
the spatial and temporal scale used to define indoor communities
will have a large impact on the processes that give rise to patterns
Figure 6. Offices in Lillis Hall show a strong distance-decay
pattern. When only considering a single space type, biological
similarity (y-axis; 1 - Canberra distance) decreases with connectance
distance (number of intermediate space boundaries [e.g., doors] one
would walk through to travel the shortest distance between any two
spaces) (Mantel test; R =0.189; P =0.002). The same pattern was also
observed at the whole-building scale (not shown; Mantel test; R =0.112;
P =0.001).
doi:10.1371/journal.pone.0087093.g006
Biogeography of Indoor Bacterial Communities
PLOS ONE | www.plosone.org 8 January 2014 | Volume 9 | Issue 1 | e87093
of diversity [26], as will the organisms being studied (e.g. bacteria
vs. fungi), and this could explain differences between our findings
and those of other recent studies [16]. For example, in a large
multi-use building with high occupant density such as Lillis Hall,
variation in human activities and uses among space types may be
the main driver of microbial community structure. In smaller
buildings with lower occupant density and stronger connections to
outdoor air sources (such as greater reliance on natural
ventilation), dispersal from outdoors may be the more important
driver of indoor microbial community structure [16].
Our study highlights network analysis as a potentially powerful
tool for applying indoor ecology and biogeography to the future of
building design. Our network analyses quantified patterns in the
form and organizations among spaces throughout Lillis Hall. From
an architectural standpoint, room arrangement within Lillis Hall
follows a double-loaded corridor design, where highly-central
circulation spaces (e.g. hallways) connect most rooms in the
building together with few intermediate spaces (radial design in
Fig. 2). This radial design strategy, compared to linear or grid
designs, reduces the range of connectance distances while
increasing the centrality (betweenness and degree) of circulation
spaces. We found that centrality was strongly correlated with
variation in microbial communities. Since increased centrality of a
space inherently increases human traffic through that space, and
both of these attributes predicted microbial community compo-
sition in the present study, our findings suggest that the
arrangement of spaces within a building is one promising way to
influence microbial community composition.
We found that design decisions can influence the ecology of
microbes within a space type - for example, in faculty offices the
source of ventilation air (window- or louver-supplied versus
mechanically-supplied ventilation) had a large impact on bacterial
community structure and the abundance of some common taxa
(e.g. Deinococcus and Methylobacterium; Fig. 5). While neither of these
genera are known to influence human health, the unusually high
abundance of the former in building dust, and particularly in
mechanically ventilated offices, gives us insight into potential
selective pressures within the built environment. Deinococcus is a
genus best known to microbiologists for the extreme oxidative
stress-, desiccation- and UV-tolerance of Deinococcus radiodurans
[27,28]. Members of this genus are commonly found in soils, on
plants, on humans, and have been detected previously in building
dust and bioaerosols, but at far lower frequency than in our study
[21,29]. It is plausible that consistently low relative humidity in
mechanically ventilated offices, as well as UV light from windows,
created indoor environmental conditions that selected for
Deinococcus in dust assemblages, while window ventilated offices
received more frequent inputs from airborne phyllosphere and soil
microbial communities, leading to higher abundances of Methylo-
bacterium.
As our understanding of the drivers of indoor microbiology
improve, it may be possible to design spaces that foster or inhibit
the growth and accumulation of different microbial taxa in order
to promote a healthier indoor microbiome. But promoting a
healthy indoor microbiome will require improved information
about the human microbiome and health. At this point our
understanding of the drivers of microbial ecology indoors has
outpaced our understanding of related health implications
[1,2,4,12,13,15,17,24,30,31]. Microbial biodiversity in the sur-
rounding environment has been linked to human health and well-
being [3234], but for the vast majority of microbial taxa, we have
no idea if their impact on our health is positive, negative, or
neutral. Considering that the indoor microbiome represents a
major potential source of microbes colonizing the human
microbiome [1,12,13], as our knowledge about commensal
microbiota expands [3539], it is foreseeable that we will be able
to target beneficial groups of indoor microbial taxa. Thus, while
future studies will be needed to understand the health implications
of indoor microbial communities, our results give clear evidence
that design choices can influence the biogeography of microbial
communities indoors, and thereby influence the interactions
between the human microbiome and the built environment
microbiome.
Conclusion
Churchill famously stated that [w]e shape our buildings, and
afterwards our buildings shape us. Humans help to direct microbial
biodiversity patterns in buildings not only as building occupants,
but also through architectural design strategies. The impact of
human design decisions in structuring the indoor microbiome
offers the possibility to use ecological knowledge to shape our
buildings in a way that will select for an indoor microbiome that
promotes our health and well-being.
Supporting Information
Figure S1 High degree of correlation between three
beta-diversity metrics. Multivariate community analysis was
carried out with the Canberra taxonomic metric; this choice
results in de-emphasis of the most abundant species (as opposed to
using the Bray-Curtis dissimilarity metric), and also ignores
nuanced evolutionary relationships between bacterial OTUs (as
opposed to using the phylogenetic Weighted UniFrac distance).
While the choice of a beta-diversity metric can impact results, the
three potential candidates that we explored resulted in largely the
same distance between samples in multivariate space. All three
metrics are bounded between 0 and 1. Pearsons correlations (r)
are given in the upper right panels.
(PNG)
Figure S2 The taxonomic composition of bacterial
communities sampled from dust in the Lillis Business
Complex. The relative abundance of sequences assigned to taxa
at different taxonomic levels is indicated by the relative width of
categories at each level. Bacterial taxonomy was visualized using
Krona (http://sourceforge.net/projects/krona/; Ondov et al.
2011).
(PDF)
Table S1 Explanation of occupancy variables.
(PDF)
Acknowledgments
We would like to thank Daniel Aughenbaugh, Laura Cavin, Keith Herkert,
Kate Laue, Alyssa Phanitdasack, Iman Rajaie and Jake Reichman for their
help during sampling. Cornelis de Kluyver, Stephanie Bosnyk, Gordon
Burke, Greg Haider, George Hecht, Don Neet, Pete Rocksvold, Frank
Sharpy and Del Smith were instrumental in assisting with building
operations and access during the study.
Author Contributions
Conceived and designed the experiments: SWK JLG BJMB DN JK.
Performed the experiments: SWK TKO GM DN MM. Analyzed the data:
SWK JFM DN JK MM. Contributed reagents/materials/analysis tools:
GZB BJMB JLG. Wrote the paper: SWK JFM JLG.
Biogeography of Indoor Bacterial Communities
PLOS ONE | www.plosone.org 9 January 2014 | Volume 9 | Issue 1 | e87093
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